Systemic autoimmunity and lymphoproliferation are associated with excess IL-7 and inhibited by IL-7Rα blockade

PLoS ONE

Volumn 6, Issue 11, 2011, Pages

  Gonzalez Quintial, Rosana ^a   Lawson, Brian R ^a   Scatizzi, John C ^a   Craft, Joseph ^b   Kono, Dwight H ^a   Baccala, Roberto ^a   Theofilopoulos, Argyrios N ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD31 ANTIGEN; CD45 ANTIGEN; CD69 ANTIGEN; CYTOKINE; HERMES ANTIGEN; INTERLEUKIN 15; INTERLEUKIN 2 RECEPTOR ALPHA; INTERLEUKIN 2 RECEPTOR BETA; INTERLEUKIN 2 RECEPTOR GAMMA; INTERLEUKIN 7; INTERLEUKIN 7 RECEPTOR; INTERLEUKIN 7 RECEPTOR ALPHA; L SELECTIN; STAT5 PROTEIN; TRANSCRIPTION FACTOR FOXP3; INTERLEUKIN 7 RECEPTOR, ALPHA CHAIN; INTERLEUKIN-7 RECEPTOR, ALPHA CHAIN; MESSENGER RNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AUTOIMMUNITY; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; DOWN REGULATION; FLOW CYTOMETRY; HOMEOSTASIS; IMMUNOBLOTTING; LYMPHADENOPATHY; LYMPHOCYTE PROLIFERATION; MEMORY T LYMPHOCYTE; MOUSE; NONHUMAN; PHENOTYPE; RECEPTOR BLOCKING; RETICULUM CELL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; T LYMPHOCYTE ACTIVATION; ANIMAL; C57BL MOUSE; DRUG ANTAGONISM; ENZYME LINKED IMMUNOSORBENT ASSAY; GENETICS; IMMUNOLOGY; LYMPHATIC SYSTEM DISEASE; LYMPHOCYTE ACTIVATION; METABOLISM; MURPHY ROTHS LARGE LYMPHOPROLIFERATIVE MOUSE; REAL TIME POLYMERASE CHAIN REACTION; T LYMPHOCYTE; WESTERN BLOTTING;

MUS;

ANIMALS; AUTOIMMUNITY; BLOTTING, WESTERN; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; INTERLEUKIN-7; LYMPHATIC DISEASES; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED C57BL; MICE, INBRED MRL LPR; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTORS, INTERLEUKIN-7; RNA, MESSENGER; T-LYMPHOCYTES;

EID: 80755152347     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0027528     Document Type: Article

References (56)

1. Surh CD, Sprent J, (2008) Homeostasis of naive and memory T cells. Immunity 29: 848-862.
2. Takada K, Jameson SC, (2009) Naive T cell homeostasis: from awareness of space to a sense of place. Nat Rev Immunol 9: 823-832.
3. Link A, Vogt TK, Favre S, Britschgi MR, Acha-Orbea H, et al. (2007) Fibroblastic reticular cells in lymph nodes regulate the homeostasis of naive T cells. Nat Immunol 8: 1255-1265.
4. Junt T, Scandella E, Ludewig B, (2008) Form follows function: lymphoid tissue microarchitecture in antimicrobial immune defence. Nat Rev Immunol 8: 764-775.
5. Mazzucchelli R, Durum SK, (2007) Interleukin-7 receptor expression: intelligent design. Nat Rev Immunol 7: 144-154.
6. Ma A, Koka R, Burkett P, (2006) Diverse functions of IL-2, IL-15, and IL-7 in lymphoid homeostasis. Annu Rev Immunol 24: 657-679.
7. Ge Q, Rao VP, Cho BK, Eisen HN, Chen J, (2001) Dependence of lymphopenia-induced T cell proliferation on the abundance of peptide/MHC epitopes and strength of their interaction with T cell receptors. Proc Natl Acad Sci U S A 98: 1728-1733.
8. Kassiotis G, Zamoyska R, Stockinger B, (2003) Involvement of avidity for major histocompatibility complex in homeostasis of naive and memory T cells. J Exp Med 197: 1007-1016.
9. Murali-Krishna K, Ahmed R, (2000) Cutting edge: naive T cells masquerading as memory cells. J Immunol 165: 1733-1737.
10. Goldrath AW, Luckey CJ, Park R, Benoist C, Mathis D, (2004) The molecular program induced in T cells undergoing homeostatic proliferation. Proc Natl Acad Sci U S A 101: 16885-16890.
11. Cho BK, Rao VP, Ge Q, Eisen HN, Chen J, (2000) Homeostasis-stimulated proliferation drives naive T cells to differentiate directly into memory T cells. J Exp Med 192: 549-556.
12. Dummer W, Niethammer AG, Baccala R, Lawson BR, Wagner N, et al. (2002) T cell homeostatic proliferation elicits effective antitumor autoimmunity. J Clin Invest 110: 185-192.
13. Hamilton SE, Wolkers MC, Schoenberger SP, Jameson SC, (2006) The generation of protective memory-like CD8+ T cells during homeostatic proliferation requires CD4+ T cells. Nat Immunol 7: 475-481.
14. Theofilopoulos AN, Dummer W, Kono DH, (2001) T cell homeostasis and systemic autoimmunity. J Clin Invest 108: 335-340.
15. Stockinger B, Kassiotis G, Bourgeois C, (2004) Homeostasis and T cell regulation. Curr Opin Immunol 16: 775-779.
16. Baccala R, Theofilopoulos AN, (2005) The new paradigm of T-cell homeostatic proliferation-induced autoimmunity. Trends Immunol 26: 5-8.
17. Krupica T Jr, Fry TJ, Mackall CL, (2006) Autoimmunity during lymphopenia: a two-hit model. Clin Immunol 120: 121-128.
18. Min B, Yamane H, Hu-Li J, Paul WE, (2005) Spontaneous and homeostatic proliferation of CD4 T cells are regulated by different mechanisms. J Immunol 174: 6039-6044.
19. Kieper WC, Troy A, Burghardt JT, Ramsey C, Lee JY, et al. (2005) Recent immune status determines the source of antigens that drive homeostatic T cell expansion. J Immunol 174: 3158-3163.
20. Tajima M, Wakita D, Noguchi D, Chamoto K, Yue Z, et al. (2008) IL-6-dependent spontaneous proliferation is required for the induction of colitogenic IL-17-producing CD8+ T cells. J Exp Med 205: 1019-1027.
21. Feng T, Wang L, Schoeb TR, Elson CO, Cong Y, (2010) Microbiota innate stimulation is a prerequisite for T cell spontaneous proliferation and induction of experimental colitis. J Exp Med 207: 1321-1332.
22. Goldrath AW, Bogatzki LY, Bevan MJ, (2000) Naive T cells transiently acquire a memory-like phenotype during homeostasis-driven proliferation. J Exp Med 192: 557-564.
23. Theofilopoulos AN, Dixon FJ, (1985) Murine models of systemic lupus erythematosus. Adv Immunol 37: 269-390.
24. Park JH, Yu Q, Erman B, Appelbaum JS, Montoya-Durango D, et al. (2004) Suppression of IL7Ralpha transcription by IL-7 and other prosurvival cytokines: a novel mechanism for maximizing IL-7-dependent T cell survival. Immunity 21: 289-302.
25. Landolfi MM, Van Houten N, Russell JQ, Scollay R, Parnes JR, et al. (1993) CD2-CD4-CD8- lymph node T lymphocytes in MRL lpr/lpr mice are derived from a CD2+CD4+CD8+ thymic precursor. J Immunol 151: 1086-1096.
26. Jevnikar AM, Grusby MJ, Glimcher LH, (1994) Prevention of nephritis in major histocompatibility complex class II-deficient MRL-lpr mice. J Exp Med 179: 1137-1143.
27. Koh DR, Ho A, Rahemtulla A, Fung-Leung WP, Griesser H, et al. (1995) Murine lupus in MRL/lpr mice lacking CD4 or CD8 T cells. Eur J Immunol 25: 2558-2562.
28. Mixter PF, Russell JQ, Durie FH, Budd RC, (1995) Decreased CD4-CD8- TCR-alpha beta + cells in lpr/lpr mice lacking beta 2-microglobulin. J Immunol 154: 2063-2074.
29. Maldonado MA, Eisenberg RA, Roper E, Cohen PL, Kotzin BL, (1995) Greatly reduced lymphoproliferation in lpr mice lacking major histocompatibility complex class I. J Exp Med 181: 641-648.
30. Christianson GJ, Blankenburg RL, Duffy TM, Panka D, Roths JB, et al. (1996) beta2-microglobulin dependence of the lupus-like autoimmune syndrome of MRL-lpr mice. J Immunol 156: 4932-4939.
31. Balomenos D, Rumold R, Theofilopoulos AN, (1997) The proliferative in vivo activities of lpr double-negative T cells and the primary role of p59fyn in their activation and expansion. J Immunol 159: 2265-2273.
32. Leonard WJ, Spolski R, (2005) Interleukin-21: a modulator of lymphoid proliferation, apoptosis and differentiation. Nat Rev Immunol 5: 688-698.
33. Rethi B, Fluur C, Atlas A, Krzyzowska M, Mowafi F, et al. (2005) Loss of IL-7Ralpha is associated with CD4 T-cell depletion, high interleukin-7 levels and CD28 down-regulation in HIV infected patients. Aids 19: 2077-2086.
34. Lang KS, Recher M, Navarini AA, Harris NL, Lohning M, et al. (2005) Inverse correlation between IL-7 receptor expression and CD8 T cell exhaustion during persistent antigen stimulation. Eur J Immunol 35: 738-745.
35. Sudo T, Nishikawa S, Ohno N, Akiyama N, Tamakoshi M, et al. (1993) Expression and function of the interleukin 7 receptor in murine lymphocytes. Proc Natl Acad Sci U S A 90: 9125-9129.
36. Fortner KA, Budd RC, (2005) The death receptor Fas (CD95/APO-1) mediates the deletion of T lymphocytes undergoing homeostatic proliferation. J Immunol 175: 4374-4382.
37. Dooms H, Wolslegel K, Lin P, Abbas AK, (2007) Interleukin-2 enhances CD4+ T cell memory by promoting the generation of IL-7R alpha-expressing cells. J Exp Med 204: 547-557.
38. Aranami T, Iclozan C, Iwabuchi K, Onoe K, (2004) IL-7-dependent homeostatic proliferation in the presence of a large number of T cells in gld mice. Microbiol Immunol 48: 477-484.
39. Henriques CM, Rino J, Nibbs RJ, Graham GJ, Barata JT, (2010) IL-7 induces rapid clathrin-mediated internalization and JAK3-dependent degradation of IL-7Ralpha in T cells. Blood 115: 3269-3277.
40. Altman A, (1994) Abnormal antigen receptor-initiated signal transduction in lpr T lymphocytes. Semin Immunol 6: 9-17.
41. Kerdiles YM, Beisner DR, Tinoco R, Dejean AS, Castrillon DH, et al. (2009) Foxo1 links homing and survival of naive T cells by regulating L-selectin, CCR7 and interleukin 7 receptor. Nat Immunol 10: 176-184.
42. Herber D, Brown TP, Liang S, Young DA, Collins M, et al. (2007) IL-21 has a pathogenic role in a lupus-prone mouse model and its blockade with IL-21R.Fc reduces disease progression. J Immunol 178: 3822-3830.
43. Elsaesser H, Sauer K, Brooks DG, (2009) IL-21 is required to control chronic viral infection. Science 324: 1569-1572.
44. Erard F, Wild MT, Garcia-Sanz JA, Le Gros G, (1993) Switch of CD8 T cells to noncytolytic CD8-CD4- cells that make TH2 cytokines and help B cells. Science 260: 1802-1805.
45. Zhang L, Fung-Leung W, Miller RG, (1995) Down-regulation of CD8 on mature antigen-reactive T cells as a mechanism of peripheral tolerance. J Immunol 155: 3464-3471.
46. Park JH, Adoro S, Lucas PJ, Sarafova SD, Alag AS, et al. (2007) 'Coreceptor tuning': cytokine signals transcriptionally tailor CD8 coreceptor expression to the self-specificity of the TCR. Nat Immunol 8: 1049-1059.
47. Cowley SC, Hamilton E, Frelinger JA, Su J, Forman J, et al. (2005) CD4-CD8- T cells control intracellular bacterial infections both in vitro and in vivo. J Exp Med 202: 309-319.
48. Maldonado MA, Kakkanaiah V, MacDonald GC, Chen F, Reap EA, et al. (1999) The role of environmental antigens in the spontaneous development of autoimmunity in MRL-lpr mice. J Immunol 162: 6322-6330.
49. Brenchley JM, Price DA, Schacker TW, Asher TE, Silvestri G, et al. (2006) Microbial translocation is a cause of systemic immune activation in chronic HIV infection. Nat Med 12: 1365-1371.
50. Bidere N, Su HC, Lenardo MJ, (2006) Genetic disorders of programmed cell death in the immune system. Annu Rev Immunol 24: 321-352.
51. Bristeau-Leprince A, Mateo V, Lim A, Magerus-Chatinet A, Solary E, et al. (2008) Human TCR alpha/beta+ CD4-CD8- double-negative T cells in patients with autoimmune lymphoproliferative syndrome express restricted Vbeta TCR diversity and are clonally related to CD8+ T cells. J Immunol 181: 440-448.
52. Crispin JC, Tsokos GC, (2009) Human TCR-alpha beta+ CD4- CD8- T cells can derive from CD8+ T cells and display an inflammatory effector phenotype. J Immunol 183: 4675-4681.
53. Liu YJ, Soumelis V, Watanabe N, Ito T, Wang YH, et al. (2007) TSLP: an epithelial cell cytokine that regulates T cell differentiation by conditioning dendritic cell maturation. Annu Rev Immunol 25: 193-219.
54. Astrakhan A, Omori M, Nguyen T, Becker-Herman S, Iseki M, et al. (2007) Local increase in thymic stromal lymphopoietin induces systemic alterations in B cell development. Nat Immunol 8: 522-531.
55. Peng SL, Madaio MP, Hayday AC, Craft J, (1996) Propagation and regulation of systemic autoimmunity by gammadelta T cells. J Immunol 157: 5689-5698.
56. Andrews BS, Eisenberg RA, Theofilopoulos AN, Izui S, Wilson CB, et al. (1978) Spontaneous murine lupus-like syndromes. Clinical and immunopathological manifestations in several strains. J Exp Med 148: 1198-1215.